Effect of Voluntary Wheel Running on Striatal Dopamine ... · Research Article Effect of Voluntary...

Research ArticleEffect of Voluntary Wheel Running on Striatal DopamineLevel and Neurocognitive Behaviors after Molar Loss in Rats

Linlin Zhang,1 Yi Feng,2 Wenliang Ji,1 Jianzhang Liu,3 and Kun Liu1,4

1Capital University of Physical Education and Sports, Beijing 100191, China2Beijing Xicheng District Desheng Community Health Service Center, Beijing 100120, China3Peking University School and Hospital of Stomatology, Beijing 100081, China4Department of Psychiatry, Yale University School of Medicine, New Haven, CT 06511, USA

Correspondence should be addressed to Jianzhang Liu; [email protected] and Kun Liu; [email protected]

Linlin Zhang and Yi Feng contributed equally to this work.

Received 9 June 2017; Revised 25 August 2017; Accepted 2 October 2017; Published 5 December 2017

Academic Editor: Francesca Trojsi

Copyright © 2017 Linlin Zhang et al. This is an open access article distributed under the Creative Commons Attribution License,which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

The aim of the present study is to evaluate the effect of voluntary wheel running on striatal dopamine level and behavior ofcognition and emotion in molar loss rats. Twenty-four Sprague-Dawley rats were enrolled in this study and randomly dividedinto following 4 groups: control group (C group), molar loss group (ML group), 1-week physical exercise before molar lossgroup (1W-ML group), and 4-week physical exercise before molar loss group (4W-ML group). The rats both in 4W-ML and1W-ML groups were placed in the voluntary running wheel in order to exercise for 4 weeks and 1 week, respectively. Then, therats in 4W-ML, 1W-M, and ML groups received bilateral molar loss operation. After 10 days, striatal dopamine level wasdetected by in vivo microdialysis coupled with high-performance liquid chromatography (HPLC) and electrochemical detection.All the rats received behavior test after microdialysis detection. The behavior tests including passive avoidance test were used toassess cognition and elevated plus maze test for emotion. The results indicated that voluntary wheel running promoted striataldopamine level in rats of molar loss. Behavioral data indicated that voluntary wheel running promoted cognition and emotionrecovery after molar loss. Therefore, we concluded physical exercise significantly improved the neurocognitive behaviors andincreased the striatal dopamine level after molar loss in rats.

1. Introduction

It is well established that tooth loss is a known risk factor ofAlzheimer’s disease (AD) [1]. As a common disorder insenior population, loss of teeth could adversely affect humancognition and emotion [2, 3]. Clinical medicine has estab-lished that tooth loss in patients can induce neuronal cell lossand memory impairment [4, 5]. Animal research also dem-onstrated that molar loss can cause the functional deteriora-tion of cognition [6]. Previous studies have demonstratedthat the rat with molar loss broke the balance of the choliner-gic neuronal system and caused the impairment of cognition[7]. In addition, a preliminary quantitative study revealedthat wide range of emotional effects was caused by tooth loss,such as loss of self-confidence and anxiety [8]. Further stud-ies have shown that physical exercise, aerobic fitness exercise

in particularly, had a positive effect on multiple aspects ofbrain function [9–11]. Neurochemistry studies indicated thatphysical exercise increased the antioxidant ability andglucose level to enhance cognition and emotion [12–14].Neurobiology research also confirmed that aerobic exercisepredominately employed the action of BDNF and the newgrowth of synaptic plasticity [15–17]. In addition, dopamineacts as a classic neurotransmitter in the brain, which plays animportant role in cognitive and emotive aspects [18–20].Numerous studies have shown that dopamine degenerationcaused significant alteration in cognitive and emotive func-tion by medicating striatal dopamine pathways [21-22].Striatum is one of the four major dopamine pathways inthe brain, partially involved in reward and in the reinforce-ment of memory consolidation. Degeneration of dopamine-producing neurons in striatum complex leads to diminished

HindawiBehavioural NeurologyVolume 2017, Article ID 6137071, 6 pageshttps://doi.org/10.1155/2017/6137071

https://doi.org/10.1155/2017/6137071

concentrations of dopamine in the nigrostriatal pathway,leading to reduce function and the characteristic symptoms,such as motor ability and cognitive impairment [23–25].Therefore, this study was designed to explore the effect ofvoluntary wheel running on striatal dopamine level and neu-rocognitive behaviors after molar loss in rats. These findingsmay provide a theoretical basis for the clinical prevention ofAlzheimer’s disease.

2. Materials and Methods

2.1. Animals. Adult male Sprague-Dawley rats (3 monthsof age, weighting 300± 50 g at the time of surgery) wereobtained from Experimental Animal Center of PekingUniversity. Rats (n = 24) were enrolled in this study andrandomly divided into following 4 groups: control group(C group, n = 6), molar loss group (ML group, n = 6),1-week physical exercise before molar loss group (1W-MLgroup, n = 6), and 4-week physical exercise before molar lossgroup (4W-ML group, n = 6). The rats in both 4W-ML and1W-ML groups were placed in the voluntary running wheelin order to exercise for 4 weeks or 1 week. Then, the rats in4W-ML, 1W-ML, and ML groups received bilateral molarloss operation. In the C group, bilateral maxillary molar teethremained intact. All rats were housed under 12 h light/darkcycle and had a sufficient amount of food and water.

2.2. Voluntary Wheel Running. The rats in both 4W-ML and1W-ML groups received voluntary wheel running. Two ratgroups were given free access to running wheels (wheelcircumference, 100 cm; Harvard Apparatus) in their cagesfor 4 weeks or 1 week. A magnetic counter was installed tothe running wheel in order to record wheel revolutions[26]. The distance was obtained by wheel revolutionsmultiplied by the circumference of the wheel. Those rats thatcannot adapt new circumstances will be removed.

2.3. Molar Loss Surgery. Bilateral maxillary molar teeth wereextracted from rats in the 4W-ML, 1W-ML, and ML groupsafter being anesthetized with chloral hydrate (350mg/kg,i.p.). The rats in the C group were anesthetized, but no teethwere extracted. To provide a suitable recovery time afterteeth extraction, experimental dentures were fitted to rats.Experimental dentures were produced from an impressionmade of silicone impression material and a resin tray.Occlusal adjustments were made until maxillomandibularincisor contacts were obtained [27].

2.4. In Vivo Microdialysis and High-Performance LiquidChromatography. In vivo microdialysis was performed byimplanting microdialysis probe into the striatum throughthe guide cannula by continuously perfusing with artificialcerebrospinal fluid (126mM NaCl, 2.4mM KCl, 1.1mMCaCl2, 0.85mMMgCl2, 27.5mM NaHCO3, 0.5mM Na2SO4,and 0.5mM KH2PO4, pH=7.0) at a flow rate of 2μL/mindriven by a microinjection pump (CMA/100, CMAMicrodi-alysis AB, Stockholm, Sweden). After 90min, microdialysatein the striatum were collected for 60 minutes; each samplewas collected in a 250μL tubes for 10min for a total of 6 tubes.Each tube was placed in an ice box containing 15 L of 10mmol

HCL. Then, dopamine level in the samples was measuredusing HPLC with electrochemical detection. The flow rate ofthe mobile phase (50mM NaH2PO3, 2mM decanesulfonicacid, 0.7mM ethylenediaminetetraacetic acid, 11% v/vacetonitrile, and 11% v/vmethanol, pH=6.0) was 1μL/min.

2.5. Passive Avoidance Test. Cognitive function was assessedby passive avoidance test [28]. After the learning trail, theretention test was measured 24 h after the learning trial. Eachanimal was put in an illuminated compartment, and the dooropened after 2 minutes. Latency to enter the dark compart-ment was recorded to a maximum of 300 s. Animals thatdid not enter the dark chamber during the retention test wereallotted a latency of 300 s [29].

2.6. Elevated Plus Maze Test. Emotion was assessed by ele-vated plus maze test [30]. The elevated plus maze was madeof plastic and consisted of two white open arms (25× 8 cm),two black enclosed arms (25× 8× 20 cm), and a central plat-form (8× 8× 8 cm) in the form of a cross. The maze wasplaced 50 cm above the floor. Rats were individually placedin the center with their heads directed toward one of theclosed arms. The total time spent in each arm or in the

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Figure 1: Dynamic changes of striatal dopamine level in eachgroup. ∗∗∗P < 0 01 compared with C group. ###P < 0 01 comparedwith ML group.

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Figure 2: The latency time of rats in learning trial and retentiontrial. ∗∗∗P < 0 001 compared with C group. ###P < 0 01 comparedwith ML group.

2 Behavioural Neurology

center and the total number of entries into each arm wereanalyzed by video monitoring for 5min. After 5min, ratswere removed from the maze and returned to their homecage. The maze was then cleaned with a solution of 70%ethyl alcohol and permitted to dry between tests [31].

2.7. Statistical Analysis. Data were analyzed by GraphPadPrism 5. A two-way analysis of variance (ANOVA) was usedto analyze the data. The comparison of cognition and emotionwas made with two-tailed Student’s t test.

3. Results

3.1. Dynamic Changes of Striatal Dopamine Level in EachGroup. Figure 1 shows dynamic changes of striatal dopaminelevel in each group. The dopamine level in C, ML, 1W-ML,and 4W-ML groups was 55.02± 9.05 fmol, 26.48± 6.67 fmol,50.01± 10.52 fmol, 52.34± 12.54 fmol, respectively. Com-pared with C group, the extracellular dopamine level of MLgroup significantly decreased (P < 0 001). Compared withML group, the extracellular dopamine level of 1W-ML and4W-ML group significantly increased (P < 0 001). However,the extracellular dopamine level has no significant differencebetween 1W-ML and 4W-ML groups (P > 0 05). The resultsindicated that 1-week or 4-week volunteer wheel runningincreased striatum dopamine level after molar loss.

3.2. Passive Avoidance Test. Figure 2 shows that the latencytime of passive avoidance test in each group. In learningtrial, the time in C, ML, 1W-ML, and 4W-ML group was65.5± 11.89 s, 62± 13.41 s, 66.5± 8.56 s, and 67.5± 10.27 sand 300 s, 67.5± 16.69 s, 300 s, and 300 s in retention trial.There was no significant difference in the learning trial foreach group (P > 0 05). Compared with C group, the retentiontime of ML group was significantly shorter (P < 0 001).Compared with ML group, the retention time of 1W-MLand 4W-ML groups was significantly longer (P < 0 001).

However, the retention time has no significant differencebetween 1W-ML and 4W-ML groups (P > 0 05). Theresults indicated that 1-week and 4-week volunteer wheelrunning can promote cognition after molar loss.

3.3. Elevated Plus Maze Test. Figure 3(a) shows that thetime spent of each rat groups in each arm. Compared withC group, the time spent of open arms in the ML groupwas significantly shorter (P < 0 001), adversely close arms(P < 0 01). Compared with ML group, the time spent ofopen arms in the 1W-ML and 4W-ML groups was signif-icantly longer (P < 0 001), adversely close arms (P < 0 01).However, the time spent in each arm has no differencebetween 1W-ML and 4W-ML groups (P > 0 05). Mean-while, there was no significant difference in the centralregion time for each group (P > 0 05). Figure 3(b) showsthat total number of crosses in three groups. But therewas no significant difference in the total number of crossesfor each group (P > 0 05). The results indicated that 1-weekor 4-week volunteer wheel running can promote emotionafter molar loss.

4. Discussion

Alzheimer’s disease (AD) can be considered as the mostcommon cause of cognitive dysfunction among the aged,and tooth loss might be a risk factor for Alzheimer-typedementia [32–34]. New advances have shown that tooth losscaused the decline of cognition [35–37]. Previous researchused passive avoid test to evaluate cognition, which showsthat molar loss may cause accumulation of the amyloid cas-cade in the brain that leads to cognitive impairment [38].Thus, we chose passive avoidance test to assess cognition inrats. We also choose elevated plus maze test to evaluate emo-tion. The results show that the cognition and emotion wereworse after molar loss. Therefore, we successfully establishedthe rat model of cognitive and emotive dysfunction after

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Figure 3: (a) Time spent of four rat groups in each arm. ∗∗∗P < 0 001 and ∗∗P < 0 01 compared with C group. ###P < 0 001 and ##P < 0 01compared with ML group. (b) Total number of crosses in each group.

3Behavioural Neurology

molar loss in this experiment. Previous study has shownthat molar loss-induced cognitive and emotive impair-ments are related to neural cell loss [38-39]. In this study,we also demonstrated that molar loss-induced cognitiveand emotive impairments are associated with the decreaseof striatal dopamine level. Clinical studies have demon-strated that cognitive impairment had pathophysiology ofdopamine system by the loss of midbrain neurons thatsynthesize the neurotransmitter dopamine [40-41]. Animalstudy also demonstrated that depression and anxiety mightbe associated with a specific loss of dopamine innervationin the limbic system [42]. Thus, it is reasonable to suggestthat the decrease of striatal dopamine level can be one ofthe important reason of cognitive and emotive impairmentafter molar loss.

However, therapeutic strategies for the cognitive andemotive impairment after molar loss have not been wellestablished so far. Molecular chemistry and biology highlightthe promoted effect of physical exercise on cognition andemotion [43–45]. Some research has shown that exerciseincreased synaptic plasticity and the level of BGF andpromoted cognition [46-47]. Other research also have shownthat exercise can enhance cell proliferation, thereby alleviat-ing anxiety-like behavior and improve emotion [48-49].Especially, studies also indicated that physical exercise, vol-untary wheel running in particularly, can be one of the bestways to promote cognition and emotion [50-51]. So, thepresent study chose voluntary wheel running as interventionapproach. Our behavioral data indicated that voluntarywheel running promoted cognitive and emotive recoveryafter molar loss. As reported previously, physical exercisepromoted the new growth of synaptic plasticity and the levelof brain glucose and improve cognition and emotion thereaf-ter [52–54]. In our research, we demonstrate that 4-week and1-week voluntary wheel running promoted cognitive andemotive recovery after molar loss is associated with theincrease of striatal dopamine level. Previous studies havedemonstrated that physical exercise increased antioxidantdefense and dopamine levels [55–57]. The increased dopa-mine level is related to recovery of cognitive and emotiveimpairments. Thus, we suggest that the increased of striataldopamine level can be one of the reasons to induce thatvoluntary wheel running promotes cognition and emotionafter molar loss in rats.

It is worth to mention that there was no differencebetween 4 weeks and 1 week of physical exercise-promotedcognition and emotion after molar loss in dopamine concen-tration aspect. Since previous research have found that smallamount of physical exercise could be beneficial to cognitivefunction, it is reasonable that 1 week of physical exercise isenough to promote cognition and emotion after molar lossin dopamine concentration aspect. Although we did not finddifference of dopamine level in striatum after 1 week and 4weeks of physical exercise in our experiment condition, it isstill possible that dopamine dynamic change in differentbrain regions could be induced by different physical exerciseprocesses. In addition, whether there is difference in otheraspects, such as other cognitive behavioral models or cellularlevels, needs to be studied further.

5. Conclusions

Physical exercise significantly promoted the cognition andemotion in rats of molar loss by increasing the striataldopamine level. However, it is necessary to further studyother neurochemicals related to dopaminergic system toelucidate more underlying mechanisms of physical exercise-promoted cognition and emotion after molar loss.

Conflicts of Interest

The authors declare that there is no conflict of interests.

Acknowledgments

The authors gratefully acknowledge the financial support byNSF of China (Grant no. 21475089), Innovation Platformof Beijing Municipality (PXM2015_014206_000053, PXM2015_014206_000072, and PXM2015_014206_000051).

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